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The Two Giant Sister Species of the Southern Ocean, Dissostichus

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The Two Giant Sister Species of the Southern Ocean, Dissostichus Polar Biol DOI 10.1007/s00300-006-0222-6 ORIGINAL PAPER The two giant sister species of the Southern Ocean, Dissostichus eleginoides and Dissostichus mawsoni, diVer in karyotype and chromosomal pattern of ribosomal RNA genes L. Ghigliotti · F. Mazzei · C. Ozouf-Costaz · C. Bonillo · R. Williams · C.-H. C. Cheng · E. Pisano Received: 5 July 2006 / Revised: 27 September 2006 / Accepted: 28 September 2006 © Springer-Verlag 2006 Abstract The two giant notothenioid species, the ping to its additional submetacentric chromosome. The Patagonian toothWsh Dissostichus eleginoides and the additional rRNA genes in D. mawsoni may be a cold- Antarctic toothWsh D. mawsoni, are important com- adaptive compensatory mechanism for growth and ponents of the Antarctic ichthyofauna and heavily development of this large species in freezing seawater. exploited commercially. They have similar appear- ance and size, both are piscivorous and bentho- Keywords Antarctica · Chromosomes · Dissostichus · pelagic, but diVer in their geographic distribution and Ribosomal genes · ToothWsh absence/presence of the antifreeze trait. We karyo- typed these two sister species by analyzing specimens collected from multiple Antarctic and sub-Antarctic Introduction sites. Both species have a diploid number of 48, but diVer in karyotypic formula, (2m + 2sm + 44a) for D. The two species of toothWsh, the Patagonian toothWsh, eleginoides and (2m + 4sm + 42a) for D. mawsoni, Dissostichus eleginoides Smitt 1898, and the Antarctic due to an extra pair of submetacentric chromosomes toothWsh, D. mawsoni Norman 1937, are important in the latter. Chromosomal Xuorescence in situ components of the Southern Ocean ichthyofauna (Gon hybridization with rDNA probes revealed unex- and Heemstra 1990). They are similar in appearance, pected species-speciWc organization of rRNA genes; body size (»100 kg), piscivory and bentho-pelagic life D. mawsoni possesses two rDNA loci (versus one style (Eastman and DeVries 2000; Horn 2002). Both locus in D. eleginoides), with the second locus map- species are usually caught between 200 and 2,000 m depth (Hanchet et al. 2003), but diVer in geographic distribution. D. eleginoides is largely subantarctic and L. Ghigliotti · F. Mazzei · E. Pisano (&) occurs in the Ross Sea, along the Antarctic Peninsula, Department of Biology, University of Genova, around subantarctic islands in the Atlantic and Indian Viale Benedetto XV 5, 16132 Genova, Italy sectors of the Southern Ocean, and on the continental e-mail: [email protected] shelf oV the coasts of Uruguay, Argentina and Chile C. Ozouf-Costaz · C. Bonillo (Brickle et al. 2005). Conversely, D. mawsoni occurs Département Systématique et Evolution, around mainland Antarctica, generally south of 60°S CNRS UMR 7138, Museum National d’Histoire Naturelle, (DeWitt et al. 1990). The distribution of the two spe- 43 rue Cuvier, 75005 Paris, France cies overlaps north of the Ross Sea, in CCAMLR R. Williams (Commission for the Conservation of Antarctic Marine Antarctic Division, Channel Highway, Living Resources) Subarea 88.1 (Horn 2002) and on Kingston, TAS 7050, Australia BANZARE Bank, i.e. the southern part of the Ker- guelen Plateau in CCAMLR Division 58.4.3b C.-H. C. Cheng Department of Animal Biology, University of Illinois, (CCAMLR 2006). Confusion over species identity in 515 Morrill Hall, Urbana, IL 61801, USA some areas has sometimes been noticed, mainly oV the 123 Polar Biol South Orkney/Antarctic Peninsula and the Southern the Weddell Sea (Ozouf-Costaz et al. 1991). The iden- Kerguelen Plateau (Fischer and Hureau 1985; Gon and tiWcation of the homologous chromosome pairs in this Heemstra 1990). specimen was diYcult due to the poor quality of the The two Dissostichus species are the major Wsh sample, but the diploid number and karyotypic for- resource exploited in the Southern Ocean by interna- mula could be determined and they are identical to tional longline and trawl Wsheries, with signiWcant those of the D. eleginoides (Ozouf-Costaz et al. 1991). international management eVorts under CCAMLR In the present work we deWne the speciWc chromo- jurisdiction (Eastman and DeVries 2000; Hanchet some set of each of the two toothWsh species by using et al. 2003; Duhamel et al. 2005). Recent escalation in conventional karyotyping and molecular cytogenetics commercial Wshing ventures, directed speciWcally and provide for the Wrst time an accurate description of towards the Antarctic toothWsh, has increased concerns the basic chromosomal features of these two important over the sustainability of the D. mawsoni Wshery, due Wsh species. This was accomplished by examining the to the scant ecological and life history information chromosome set of several specimens of both sexes, available on this species (Parker et al. 2002; Hanchet collected from multiple Antarctic and sub-Antarctic et al. 2003). locations. A more in-depth characterization was Physiologically, the two species diVer notably in their obtained through cytogenetic mapping of ribosomal capability to live at subzero temperatures. D. mawsoni genes by Xuorescence in situ hybridization (FISH), has a large family of antifreeze glycoprotein (AFGP) which revealed unexpected species-speciWc patterns in genes and produces high levels of circulatory AFGPs these two sister taxa. that prevent the freezing of its body Xuids (Chen et al. In the broader context of comparative genomics, the 1997; DeVries and Cheng 2005). In contrast, D. elegino- cytogenetic data presented here provide the necessary ides has barely detectable AFGP sequences in its DNA, basis for approaching further analyses of the genomes and no antifreeze activity in its blood (Cheng and of these two important species through the visualiza- Detrich 2006). This distinct diVerence is consistent with tion of gene loci at the chromosomal level. The use of the separate geographic distribution of the two tooth- speciWc DNA or gene sequences as probes in chromo- Wsh in freezing versus non-freezing habitats. The evolu- somal FISH is a powerful tool that provides spatial tionary history of these two species in disparate thermal landmarks and linkage information in a genome that environments suggests other signiWcant molecular and can help resolve positional ambiguities in whole biological diVerences are likely to exist, despite their genome sequence assemblies, as well as facilitate the close phylogenetic kinship. elucidation of gene family and genome organizations Taxonomically, the genus Dissostichus belongs to and evolution (Cheung et al. 2001; Jaillon et al. 2004). Nototheniidae, the most diversiWed family of the sub- order Notothenioidei, and it is presently included in the subfamily Pleuragrammatinae (Balushkin 2000) Materials and methods together with the other pelagic genera Pleuragramma, Aethotaxis and Gvozdarus. According to phylogenetic Animal sampling and chromosome preparation analyses, Dissostichus is a basal nototheniid lineage. Using penalized likelihood analysis combined with fos- Specimens of D. eleginoides were collected in the sil calibration, the age of most recent common ancestor Indian and Atlantic sectors of the Southern Ocean. of the two Dissostichus species was estimated to be The specimens from the Indian sector (four females, about 14.5 My (Near 2004). three males and one undetermined juvenile) were Despite substantial scientiWc attention to the tooth- caught by use of bottom trawls during the “Thirst” Wsh related to biodiversity conservation, Wshery man- Cruise 1993 aboard the Australian R/V Aurora Aus- agement (Parker et al. 2002; Hanchet et al. 2003) and tralis (around 51°/52°S, 72°/75°E). The specimens from molecular analyses of the antifreeze trait (Chen et al. the Atlantic sector (six females) were collected by 1997; Cheng and Detrich 2006), cytogenetic analyses of traps during the “ICEFISH” Cruise 2004 aboard the the two species are presently scanty. On the basis of a United States R/V Nathaniel B. Palmer (at 54°S, 55°W single juvenile caught oV the Kerguelen Islands, Dous- approximately). sau De Bazignan and Ozouf-Costaz (1985) provided Specimens of D. mawsoni, two males and two preliminary data on the diploid number (48) and females, were collected in McMurdo Sound (78°S, karyotypic formula (44a + 2sm + 2m) of D. eleginoides. 167°E) by winched cable and hook through large holes For D. mawsoni, the only available karyotypic infor- drilled through sea ice. Other specimens were caught mation is based on the analysis of a single female from by bottom trawls during the Western Ross Sea Voyage 123 Polar Biol 2004 aboard the New Zealand R/V Tangaroa, one Wcation of genomic DNA. On the basis of Notothenia female in the Ross Sea (at 72°S, 173°E approximately) coriiceps 28S ribosomal DNA partial sequences (Gen- and two females around the Balleny Islands (67°S, Bank accession numbers AY141673 and AY141674), a 164°E). Six specimens (females) were caught by gill pair of primers, Noto_28S_C1 For (5Ј-CTA ACC nets at the French Station Dumont D’Urville (Adélie AGG ATT CCC TCA GTA GCG G-3Ј) and Land) (64°S, 140°E). Noto_28S_D3 Rev (5Ј-CAG GCA TAG TTC ACC Specimens were maintained in tanks or aquaria sup- ATC TTT CGG GTC-3Ј) were designed for ampliWca- plied with fresh, aerated seawater at local ambient tion. The PCR product was cloned in the pGEM-T temperature aboard the scientiWc vessels or at the Ant- Easy vector (Promega) and sequenced with BigDye v.3 arctic science stations. Specimens were injected with chemistry (Applied Biosystems). The sequence of colchicine and mitotic cells were obtained
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